Collective personalities: present knowledge and new frontiers

Wright, Colin M.; Lichtenstein, James L. L.; Doering, Grant Navid; Pretorius, Justin; Meunier, Joël; Pruitt, Jonathan N.

doi:10.1007/s00265-019-2639-2

Cited by 36 publications

(47 citation statements)

References 256 publications

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“…Collective behavior is ubiquitous in nature and presumed to have strong fitness consequences for group members. Moreover, repeatable variation in collective behavior (often described as collective or group-level "personality") has been commonly observed (Bengston & Jandt 2014;Planas-Sitjà et al 2015;Jolles et al 2017;Wright et al 2019). However, we still know little about the underlying genetic mechanisms generating variation in collective behavior and how collective behavior is shaped by selection.…”

Section: Discussionmentioning

confidence: 99%

“…Researchers are increasingly interested in documenting patterns of variation in collective behavior between groups (i.e. describing collective or group personality; Jandt et al 2014;Bengston & Jandt 2014;Wright et al 2019) with a goal of understanding the evolutionary causes and consequences of variation in collective behavior. However, the degree to which collective behaviors are heritable and how genetic variation contributes to population-level variation in individual and collective behaviors remains largely unknown.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, it is often assumed that, like individual behavior and other individual-level traits, collective behavior and other group-level traits are strongly shaped by natural selection (Gordon 2013(Gordon , 2016. However, very little is actually known about how natural selection acts on collective behaviors or group-level traits more generally (Wright et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Ant collective behavior is heritable and shaped by selection

Walsh

Garnier

Linksvayer

2019

Preprint

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11Collective behaviors are widespread in nature and usually assumed to be strongly shaped 12 by natural selection. However, the degree to which variation in collective behavior is heritable 13 and has fitness consequences --the two prerequisites for evolution by natural selection --is 14 largely unknown. We used a new pharaoh ant (Monomorium pharaonis) mapping population to 15 estimate the heritability, genetic correlations, and fitness consequences of three collective 16 behaviors (foraging, aggression, and exploration) as well as body size, sex ratio, and caste ratio. 17Heritability estimates for the collective behaviors were moderate, ranging from 0.17 to 0.32, but 18 lower than our estimates for the heritability of caste ratio, sex ratio, and the body size of new 19 workers, queens, and males. Moreover, variation among colonies in collective behaviors was 20 phenotypically correlated, suggesting that selection may shape multiple colony collective 21 behaviors simultaneously. Finally, we found evidence for directional selection that was similar in 22 strength to estimates of selection in natural populations. Altogether, our study begins to elucidate 23 the genetic architecture of collective behavior and is one of the first studies to demonstrate that it 24 is shaped by selection. 25

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Ant collective behavior is heritable and shaped by selection

Walsh

Garnier

Linksvayer

2019

Preprint

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“…This also points to the advantages of taking a network approach to analyzing gene expression data, in addition to traditional differential expression statistics 93,150,153 . Key general questions here include how ecological factors interact with solitary insect gene regulatory networks in order to allow for the transition to eusociality 18,154 , and in which ways these transitions toward eusociality are unique vs. universal 18,71,155 .…”

Section: Predictions For Glandsmentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

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“…Intraspecific variation provides evolutionary biologists with a useful tool to probe the selective forces that underlie the evolution of colony life-history traits and to examine how behavior shapes them (Bengston & Jandt, 2014; Jandt, Bengston, Pinter-Wollman, Pruitt, Raine, Dornhaus & Sih, 2014; Wright, Lichtenstein, Doering, Pretorius, Meunier & Pruitt, 2019). By comparing the life-history metrics of natural colonies and testing for associations between them, studies focused on intraspecific variation can provide clues as to which colony life-history traits exhibit the most variability, and whether there are conspicuous associations between them, which could hint at the presence of trade-offs or illuminate possible coadaptation between colony traits (e.g., behavior, demography, nest attributes).…”

Section: Introductionmentioning

confidence: 99%

Foundress Number, But Not Queen Size or Boldness, Predicts Colony Life-History in Wild Paper Wasps

Wright

Fisher

Nerone

et al. 2019

Preprint

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3Colonies of social insects exhibit a spectacular variety of life histories. Here we documented the 1 4 degree of variation in colony life-history traits, mostly related to productivity, in two species of 1 5 wild paper wasps. We then tested for associations between colony life-history traits to look for 1 6 trade-offs or positively associated syndromes, and examined whether individual differences in 1 7 the behavioral tendencies of foundresses (Polistes metricus) or the number of cofoundresses (P. 1 8 fuscatus) influenced colony life-history. The majority of our measures of colony life-history 1 9 were positively related, indicating no obvious resource allocation trade-offs. Instead, the positive 2 0association of traits into a productivity syndrome appears to be driven by differences in queen or 2 1 microhabitat quality. Syndrome structure differed only marginally between species. Queen 2 2 boldness and body size were not associated with colony life-history in P. metricus. Colonies 2 3 initiated by multiple P. fuscatus foundresses were generally more productive, and this advantage 2 4was approximately proportional to the number of cofoundresses. These findings demonstrate that 2 5 colony life-history traits can be associated together much like individual life-history traits, and 2 6 the associations seen here convey that differences in overall productivity drive between-colony 2 7 differences in life-history. 2 8

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Collective personalities: present knowledge and new frontiers

Cited by 36 publications

References 256 publications

Ant collective behavior is heritable and shaped by selection

Ant collective behavior is heritable and shaped by selection

Distributed physiology and the molecular basis of social life in eusocial insects

Foundress Number, But Not Queen Size or Boldness, Predicts Colony Life-History in Wild Paper Wasps

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